Muscle Synergies: Use and Validation in Clinics, Robotics, and Sports

Since understanding how the human brain generates neural commands to control muscles during motor tasks still remains an untapped question, great interest is shown in the validation and application of muscle synergies among research groups focused on the electromyography (EMG). In the last decades, the factorization of the EMG signals by means of muscle synergies has been proposed to understand the neurophysiological mechanisms related to the central nervous system ability in reducing the dimensionality of muscle control. For this reason, we planned a special issue on validation and application of the muscle synergy theory to discuss the methodological issues and to propose novel applications in clinics, robotics, and sports. The special issue achieved success among researchers as demonstrated by the large amount of submitted papers and the scientific impact of the published ones. The special issue is composed of twelve manuscripts. Three systematic reviews are included: (i) the first one is focused on the meaning of the muscle synergy theory to understand its applicability as a neurorehabilitation tool (Singh et al.); (ii) the second one is useful to understand the applications of muscle synergies in the investigation of muscle coordination during walking of poststroke patients (Seamon et al.); and (iii) the third one offers a complete overview on the tangible applications of muscle synergies in clinics, robotics, and sports (Taborri et al.). As concerns clinics, the effects of upper limb weakness and task failure, which is the inability to maintain a certain level of force during a task, on the muscle synergies are evaluated by Roh et al. and Castronovo et al., respectively. As regards robotics, the feasibility to use a muscle synergy approach to implement the control system of an upper limb exoskeleton is presented by Chiavenna et al. Moving to the sports, two papers are focused on understanding the muscle synergy organization during the execution of specific technical actions of the badminton (Matsunaga et al. and Barnamehei et al.), one paper shows the muscle synergy structure involved in stability exercises of rhythmic gymnastics (Rutkowska-Kucharska et al.), while the motor control underlying the throwing movement is studied by Cruz-Ruiz et al. Finally, two papers investigate some fundamental methodological issues; in particular concerning the influence of initialization techniques for the application of non-negative matrix factorization (Soomro et al.) and the reliability and repeatability of the methodology for extracting muscle synergies during daily life activities (Taborri et al.). We hope that this special issue can represent an important step to strengthen the use of muscle synergies to explain how the human brain organizes the muscle activation both in clinics and robotics, as well as in sports applications

Alterations in the preferred direction of individual arm muscle activation after stroke

IntroductionStroke survivors have challenges appropriately coordinating the multiple muscles, resulting in a deficit in motor control. Therefore, comprehending the mechanism underlying abnormal intermuscular coordination becomes crucial in developing effective rehabilitation strategies. Quantitative analyses have been employed at pairwise or multi-dimensional levels to understand the underlying mechanism of abnormal intermuscular coordination and its relationship to motor impairment. However, how alterations in individual muscle activation contribute to abnormal intermuscular coordination, motor impairment, and motor performance remains unclear. Thus, we investigated the alterations in the preferred direction of individual muscles after stroke and their relationship with stroke-induced changes in intermuscular coordination, clinical motor impairment, and qualities of motor performance during isometric force generation in the upper extremity.MethodsTwenty-four stroke survivors and six age-matched controls were recruited and performed isometric force target matches while recording electromyographic signals from eight upper limb muscles. We determined the preferred activation direction of each muscle, evaluated abnormal intermuscular coordination through a muscle synergy analysis, assessed motor impairment using upper extremity Fugl-Meyer Assessment scores, and examined motor performance characteristics defined by force trajectory features.ResultsThe post-stroke alterations in the preferred direction of the brachioradialis, anterior, middle, and posterior deltoid were correlated with the motor impairment level and attributed to the changes in muscle synergy characteristics. Only alterations in the preferred direction of the brachioradialis and posterior deltoid activation in forward-backward and upward-downward axes were associated with the qualities of isometric force generation, respectively.DiscussionThese findings imply that alterations in the preferred direction of individual muscle activation contribute to various aspects of motor deficit following stroke. This insight may serve as a foundation for the development of innovative stroke neurorehabilitation approaches that take into account specific attributes of individual muscle activation, including their preferred activation direction

Generalizability of muscle synergies in isometric force generation versus point-to-point reaching in the human upper extremity workspace

Isometric force generation and kinematic reaching in the upper extremity has been found to be represented by a limited number of muscle synergies, even across task-specific variations. However, the extent of the generalizability of muscle synergies between these two motor tasks within the arm workspace remains unknown. In this study, we recorded electromyographic (EMG) signals from 13 different arm, shoulder, and back muscles of ten healthy individuals while they performed isometric and kinematic center-out target matches to one of 12 equidistant directional targets in the horizontal plane and at each of four starting arm positions. Non-negative matrix factorization was applied to the EMG data to identify the muscle synergies. Five and six muscle synergies were found to represent the isometric force generation and point-to-point reaches. We also found that the number and composition of muscle synergies were conserved across the arm workspace per motor task. Similar tuning directions of muscle synergy activation profiles were observed at different starting arm locations. Between the isometric and kinematic motor tasks, we found that two to four out of five muscle synergies were common in the composition and activation profiles across the starting arm locations. The greater number of muscle synergies that were involved in achieving a target match in the reaching task compared to the isometric task may explain the complexity of neuromotor control in arm reaching movements. Overall, our results may provide further insight into the neuromotor compartmentalization of shared muscle synergies between two different arm motor tasks and can be utilized to assess motor disabilities in individuals with upper limb motor impairments

Feasibility of Muscle Synergy Outcomes in Clinics, Robotics, and Sports: A Systematic Review

In the last years, several studies have been focused on understanding how the central nervous system controls muscles to perform a specific motor task. Although it still remains an open question, muscle synergies have come to be an appealing theory to explain the modular organization of the central nervous system. Even though the neural encoding of muscle synergies remains controversial, a large number of papers demonstrated that muscle synergies are robust across different tested conditions, which are within a day, between days, within a single subject and between subjects that have similar demographic characteristics. Thus, muscle synergy theory has been largely used in several research fields, such as clinics, robotics and sports. The present systematical review aims at providing an overview on the applications of muscle synergy theory in clinics, robotics and sports; in particular, the review is focused on the papers that provide tangible information for: (i) diagnosis or pathology assessment in clinics; (ii) robot-control design in robotics; and (iii) athletes’ performance assessment or training guidelines in sports

Alterations in motor modules and their contribution to limitations in force control in the upper extremity after stroke

The generation of isometric force at the hand can be mediated by activating a few motor modules. Stroke induces alterations in motor modules underlying steady-state isometric force generation in the human upper extremity (UE). However, how the altered motor modules impact task performance (force production) remains unclear as stroke survivors develop and converge to the three-dimensional (3D) target force. Thus, we tested whether stroke-specific motor modules would be activated from the onset of force generation and also examined how alterations in motor modules would induce changes in force representation. During 3D isometric force development, electromyographic (EMG) signals were recorded from eight major elbow and shoulder muscles in the paretic arm of 10 chronic hemispheric stroke survivors and both arms of six age-matched control participants. A non-negative matrix factorization algorithm identified motor modules in four different time windows: three “exploratory” force ramping phases (Ramps 1–3; 0–33%, 33–67%, and 67–100% of target force magnitude, respectively) and the stable force match phase (Hold). Motor module similarity and between-force coupling were examined by calculating the scalar product and Pearson correlation across the phases. To investigate the association between the end-point force representation and the activation of the motor modules, principal component analysis (PCA) and multivariate multiple linear regression analyses were applied. In addition, the force components regressed on the activation profiles of motor modules were utilized to model the feasible force direction. Both stroke and control groups developed exploratory isometric forces with a non-linear relationship between EMG and force. During the force matching, only the stroke group showed abnormal between-force coupling in medial-lateral and backward-forward and medial-lateral and downward-upward directions. In each group, the same motor modules, including the abnormal deltoid module in stroke survivors, were expressed from the beginning of force development instead of emerging during the force exploration. The PCA and the multivariate multiple linear regression analyses showed that alterations in motor modules were associated with abnormal between-force coupling and limited feasible force direction after stroke. Overall, these results suggest that alterations in intermuscular coordination contribute to the abnormal end-point force control under isometric conditions in the UE after stroke

Modules in the brainstem and spinal cord underlying motor behaviors

Thesis (Ph. D.)--Massachusetts Institute of Technology, Dept. of Brain and Cognitive Sciences, 2008.This electronic version was submitted by the student author. The certified thesis is available in the Institute Archives and Special Collections.Includes bibliographical references (leaves 89-95).Previous studies using reduced or intact animal preparations suggested that coordinated movements can be generated by appropriate combinations of muscle synergies controlled by the nervous system. However, which areas of the central nervous system are responsible for structuring and combining muscle synergies remains an open question. In my thesis, I have addressed the question whether the brainstem and spinal cord are involved in structuring and combining muscle synergies in order to execute a range of natural movements. The strategy to investigate this question was to analyze the electromyogram (EMG) data recorded from the leg muscles during frog motor behaviors before and after neuronal transection. In my two sets of experiments, EMGs were recorded before and after transection at the level of the caudal end of the third ventricle and at the level of the caudal end of the pons in two groups of frogs. When the section was at the level of rostral midbrain, movements such as jumps, swims, kicks, and walks could be performed by the animals. In contrast, when the transection was at the level of rostral medulla, only a partial repertoire of natural movements could be evoked. Systematic analysis of muscle synergies in these preparations found two different types of synergies: (1) synergies shared by intact animals and animals with transection, and (2) synergies specific to individual motor behaviors. In addition, almost all synergies utilized in the execution of natural motor behaviors remain invariant after transection at the level of the caudal end of the third ventricle or at the level of the caudal end of the pons. The results suggest the following:(cont.) (1) the neural network within the brainstem and spinal cord are necessary and sufficient in combining muscle synergies in the organization of natural movements, and (2) the neural circuitries within the medulla and spinal cord are sufficient to structure the repertoire of muscle synergies in natural motor behaviors. Overall, the major findings of this study indicate how the neural divisions in the CNS are functionally differentiated for structuring and combining modules in execution of natural movements.by Jinsook Roh.Ph.D

Image_1_Generalizability of muscle synergies in isometric force generation versus point-to-point reaching in the human upper extremity workspace.pdf

Isometric force generation and kinematic reaching in the upper extremity has been found to be represented by a limited number of muscle synergies, even across task-specific variations. However, the extent of the generalizability of muscle synergies between these two motor tasks within the arm workspace remains unknown. In this study, we recorded electromyographic (EMG) signals from 13 different arm, shoulder, and back muscles of ten healthy individuals while they performed isometric and kinematic center-out target matches to one of 12 equidistant directional targets in the horizontal plane and at each of four starting arm positions. Non-negative matrix factorization was applied to the EMG data to identify the muscle synergies. Five and six muscle synergies were found to represent the isometric force generation and point-to-point reaches. We also found that the number and composition of muscle synergies were conserved across the arm workspace per motor task. Similar tuning directions of muscle synergy activation profiles were observed at different starting arm locations. Between the isometric and kinematic motor tasks, we found that two to four out of five muscle synergies were common in the composition and activation profiles across the starting arm locations. The greater number of muscle synergies that were involved in achieving a target match in the reaching task compared to the isometric task may explain the complexity of neuromotor control in arm reaching movements. Overall, our results may provide further insight into the neuromotor compartmentalization of shared muscle synergies between two different arm motor tasks and can be utilized to assess motor disabilities in individuals with upper limb motor impairments.</p